AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 112:57– 68 (2000)

Growth of Skeletal Components in the Young Squirrel Monkey

(Saimiri sciureus boliviensis): A Longitudinal Experiment
HÉCTOR M. PUCCIARELLI,1,2* MARÍA C. MUÑE,1,2
EVELIA E. OYHENART,1,2 ALICIA B. ORDEN,2 MIRIAM E. VILLANUEVA,3
RAÚL R. RODRÍGUEZ,3 AND EDUARDO R. PONS3
1
Consejo Nacional de Investigaciones Cientı́ficas y Técnicas (CONICET),
Universidad Nacional de La Plata, 1900 La Plata, Argentina
2
Centro de Investigaciones en Genética Básica y Aplicada (CIGEBA),
Universidad Nacional de La Plata, 1900 La Plata, Argentina
3
Servicio de Diagnóstico por Imágenes, Facultad de Ciencias
Veterinarias, Universidad Nacional de La Plata,
1900 La Plata, Argentina

KEY WORDS primates; nutrition; growth curves; linear equa-

tions; functional indices

ABSTRACT A functional skeletal criterion, as an extension of the van der

Klaauw’s cranial theory, was adopted in the present study. The null hypothesis
tested was: “The major skeletal components of the platyrrhine body grow lin-
early, regardless of their functional dependence to different demands.” The
acceptance of the hypothesis will imply that all Saimiri skeletal growth may be
satisfactorily explained by independent variables in a single equation. The
rejection will suggest that such skeletal growth patterns have to be explained by
variables in several different equations, and perhaps these equations may vary
with the effect of sex and undernutrition. Control and undernourished squirrel
monkeys were radiographed monthly for 2 years; they were also measured; and
their volumetric and morphometric neurocranial, facial, and pelvic indices were
calculated. The curves that best described each of the 24-point sequences were
obtained. Three main growth patterns were observed: 1) Simple linear (femur
length for all groups, and pelvic index for control and undernourished females),
for which the simple regression equation explained more than 95% of the vari-
ation; 2) Complex linear (pelvic index for control and undernourished males, and
neurocranial and facial indices for all of the groups), for which more than 95% of
the variation was explained by one of the four four-function type equations; and
3) Noncorrelated with age (neurofacial index for undernourished males, and
pelviofemoral index for control females and undernourished males and females),
which showed nonsignificant correlations with respect to age. The food intake
and the oscillations of the environmental temperature might help to explain the
undulating growth trajectory observed in the complex linear components. Am J
Phys Anthropol 112:57– 68, 2000. © 2000 Wiley-Liss, Inc.

Longitudinal studies are a useful way to

understand how humans and other mam-
mals grow from birth to adulthood. How-
ever, due to their high cost in money and
time, such studies are not frequently em-
ployed in comparative and experimental
auxology. Rather, they are replaced by the
faster, easier, and less expensive cross-sec-
Grant sponsor: CONICET; Grant sponsor: Universidad Nacio-
nal de La Plata.
*Correspondence to: Dr. Héctor M. Pucciarelli, Centro de In-
vestigaciones en Genética Básica y Aplicada (CIGEBA),
Facultad de Ciencias Veterinarias, Calles 60 y 118, Casilla
de Correo 296, 1900 La Plata, Argentina.
E-mail: hmpucci@fcv.medvet.unlp.edu.ar
Received 2 March 1998; accepted 13 December 1999.

© 2000 WILEY-LISS, INC.

58 H.M. PUCCIARELLI ET AL.
tional studies. The cross-sectional informa-
tion, however, is far from being sufficiently
accurate. The main problem with cross-sec-
tional data is that the comparisons are be-
tween the means from different individuals
at different age stages. The main advantage
of the longitudinal method is that a given
individual may act as his own control at
different growth stages. We agree with Tan-
ner (1988) that, although longitudinal stud-
ies have to be accompanied by cross-sec-
tional surveys and animal experimentation
not to become sterile, longitudinal methods
are indispensable in growth research. The
“purely longitudinal” method is the best
variant of longitudinal growth studies, be-
cause this approach requires all individuals
to share the same birthday, and thus they
are all measured simultaneously. This is
feasible in experimental animals, in which,
apart from age, all independent variables
can be kept equally controlled throughout
the analysis.
Morphologists can start researching on
craniology from two opposite paradigms.
The typological one considers the skeleton
from a merely descriptive point of view. The
other paradigm is not static and holds some
independence in the growth behavior of
skeletal components due to the functional
demands imposed by a related organ, tissue,
and/or cavity. The latter is the basic concep-
tion of the functional cranial theory postu-
lated by Klaauw (1948 –1952) in mammals
and developed by Moss and Young (1960)
and Moss (1973, 1979) for human and
nonhuman primates. The skull can be con-
sidered as composed of many functional
components, which display relative inde-
pendence among each other. The variation
of a functional cranial component (FCC) re-
flects the demands imposed by the growth of
different related structures of the head.
Each FCC is composed of a functional ma-
trix (FM) and a skeletogen unity (SKU). The
FM includes all the elements (organs, tis-
sues, nerves, functional spaces, etc.) neces-
sary to perform a function. The SKU sup-
ports and protects biomechanically its
specific FM (Moss, 1973, 1979), and should
be the object of measurement when osteolo-
gists go beyond a mere descriptive study.
This conception is specially useful for study-
ing cranial structures (Moss and Young,
1960; Pucciarelli et al., 1990), though there
is no reason for not extending it to the re-
maining parts of the skeleton. A good exam-
ple is the recent cross-sectional study made
by Humphrey (1998) on growth in humans.
According to Tanner (1988), fitting curves
in growing individuals may be an actual
muddle. Stature, for example, is composed
of several different osseous individualities
measured by height, foot, leg, thigh, pelvis,
vertebrae, and skull height. Each of these
has its own modality of growth. Fitting
curves may indeed be impossible if one has
a classical conception of the skeleton, but it
is feasible when the functional criterion is
extended to the skeletal frame. If specific
curves are adjusted to each growing compo-
nent, we will explain each functional behav-
ior by its best fitted curve. Each functional
component may be measured by specific
variables and indices which assure a degree
of homogeneity in growth behavior (Puc-
ciarelli et al., 1990; Pucciarelli and Neves,
1992; Dressino and Pucciarelli, 1997). In the
present study, the Saimiri skeleton was
studied from this functional point of view.
The growth of the neurocranium, face, and
pelvis was measured by functional indices,
together with indicators of linear (femur
length) and three-dimensional (body weight)
growth modalities.
The nearer to humans the taxonomic dis-
tance of the experimental animals, the more
useful the experiment to understand human
growth processes. In this respect, the squir-
rel monkey (Saimiri sciureus) is specially
useful in experimental studies, since, ac-
cording to several authors (Ameghino, 1909;
Biegert, 1963; Petit-Maire, 1971; Petit-
Maire et al., 1974), many morphological re-
semblances between Saimiri and Homo
genera permit generalizing our findings to
humans more than would findings in other
New World monkeys. Several mixed-longi-
tudinal (Leigh, 1996), longitudinal (Ha-
mano et al., 1990; Garber and Leigh, 1997),
and purely longitudinal (Dressino, 1991;
Dressino and Pucciarelli, 1997) studies on
growth in Saimiri species were made during
the past few years.
The present purely longitudinal study
was designed to test the null hypothesis:
 GROWTH OF SQUIRREL MONKEY SKELETAL COMPONENTS
“All major skeletal components of the
platyrrhine body grow linearly, regardless
of the functional dependence on different
demands.” If the null hypothesis is ac-
cepted, femur length and the three func-
tional components studied here have to be
explained by a single equation. If true, the
conclusion would be that the platyrrhine
skeleton is genetically hardwired and
growth changes due to the environment af-
fect it linearly. If the hypothesis is rejected,
the conclusion will point out that different
growth patterns in the skeletal frame do
exist and the environment will act differen-
tially on them. This study sets the three
following objectives as its goals: 1) to find
the equations that best describe the growth
of the different functional skeletal compo-
nents in Saimiri of both sexes; 2) to estab-
lish whether the equations that fit best in
controls are the same as in undernourished
animals; and 3) to infer if there is a relation-
ship between Saimiri growth trends and
environmental conditions of the tropical
forest.
MATERIALS AND METHODS
Ten male and ten female platyrrhine
monkeys (Saimiri sciureus boliviensis) were
born and grown in captivity at the Centro
Argentino de Primates (CAPRIM). After
weaning the males weighed, on average,
463.2 ⫾ 24.1 g and the females 412.7 ⫾
35.7 g. The animals were transferred to the
Centro de Investigaciones en Genética Bá-
sica y Aplicada (CIGEBA), and placed in
individual cages measuring 60 ⫻ 60 ⫻ 60
cm. They were fed ad libitum on a 20% pro-
tein semisynthetic diet. Each animal re-
ceived a daily supplement of 40 g of fresh
orange, and 5 ml of a 50% glucose fat-free
milk water solution. This supply lasted un-
til the end of the adaption period (1 year of
age). The animals were periodically tested
and prevented from developing parasitism
and other illnesses. When the animals were
12 months old, they were rearranged in four
groups of five: a) control males and b) con-
trol females received the 20% protein semi-
synthetic diet ad libitum, while c) under-
nourished males and d) undernourished
females received a low-protein (10%) semi-
59
synthetic diet ad libitum (see Dressino and
Pucciarelli, 1997, for details).
Two radiographs, one in strict later-lat-
eral view and the other in strict dorsi-ven-
tral view, were taken per animal/month,
from the 13th to the 36th month of age. For
this purpose, a Siemens Heliophos 4 from
the Servicio de Diagnóstico por Imágenes,
with 240 mA and 125 Kv of power, was
employed. Shoots were regulated at 100
mA; 0.02 seg; 40 –50 Kv (according to the
age of the animal). A 110cm focus-film
(AGFA 18 ⫻ 24 cm) distance was used to
reduce the magnification effect, calculated
as: MgC ⫽ Bx/Ax; where MgC ⫽ magnifica-
tion coefficient, Ax ⫽ variable measured on
the 24th month radiograph; and Bx ⫽ the
same variable measured on the skull
(Dressino and Pucciarelli, 1997). Data from
the present study were multiplied by a
MgC ⫽ 0.94 to get the actual value.
In the later-lateral view, the following
measurements were made: neurocranial
length (Nl), from nasion to opisthocranion;
neurocranial height (Nh), from basion to
bregma; face length (Fl), from prosthion to
posterior nasal spine; face height (Fh), from
nasion to gnation; pelvic length (Pl), the
maximum anterior-posterior distance mea-
sured perpendicularly to the vertebral col-
umn; pelvic height (Ph), from the highest
point of the iliac crest to the lowest point of
the pubis, and femur length (Fel), maximum
length of the femur (parallel to the caliper).
In the dorsi-ventral view, the following mea-
surements were made: neurocranial width
(Nw), bi-eurion distance; face width (Fw),
bi-zygomatic distance; and pelvis width
(Pw), maximum distance between the iliac
crests. The following functional indices were
calculated:
Neurocranial index 共Ni兲
⫽ 100 冑3 N ⴱ Nw ⴱ Nh
Facial index 共Fi兲 ⫽ 100 冑3 F ⴱ Fw ⴱ Fh
Pelvic index 共Pi兲 ⫽ 100 冑3 P ⴱ Pw ⴱ Ph
Neurofacial index 共NFi兲 ⫽ 100 ⴱ NiⲐFi
Pelviofemoral index 共PFi兲 ⫽ 100 ⴱ PiⲐFel
60 H.M. PUCCIARELLI ET AL.

TABLE 1. One-sample Kolmogorov-Smirnov (K-S) statistics for testing normality of the frequency distributions1
Control Undernourished
Male Female Male Female
DN P DN P DN P DN P
Body weight 0.148 0.617 0.148 0.669 0.135 0.776 0.118 0.895
Femur length 0.127 0.791 0.163 0.544 0.128 0.114 0.198 0.305
Neurocranial length 0.138 0.699 0.138 0.699 0.092 0.975 0.099 0.956
Neurocranial width 0.163 0.494 0.161 0.512 0.221 0.166 0.188 0.321
Neurocranial height 0.219 0.174 0.219 0.174 0.102 0.944 0.119 0.846
Facial length 0.127 0.791 0.127 0.791 0.154 0.567 0.153 0.575
Facial width 0.142 0.670 0.142 0.670 0.146 0.633 0.142 0.668
Facial height 0.103 0.938 0.103 0.938 0.132 0.748 0.138 0.698
Pelvic length 0.119 0.843 0.119 0.843 0.195 0.283 0.150 0.596
Pelvic width 0.152 0.582 0.152 0.582 0.171 0.433 0.154 0.571
Pelvic height 0.114 0.882 0.114 0.882 0.160 0.519 0.085 0.990
Neurocranial index 0.133 0.787 0.233 0.146 0.177 0.443 0.111 0.927
Facial index 0.100 0.972 0.156 0.601 0.198 0.306 0.126 0.839
Pelvic index 0.232 0.147 0.101 0.979 0.176 0.447 0.112 0.925
1
DN, result of K-S test; P, statistical probability. P ⬎ 0.05 means that the frequency distribution is symmetric.

The femur length was used as an indica-
tor of growth in stature. The first three in-
dices are called volumetric, since they detect
size plus shape changes (Pucciarelli et al.,
1990); they were expressed as the cubic root
in order to compare the three-dimensionally
measured components with chronological
age. The same procedure was followed for
body weight. The last two indices are called
morphometric, since they detect only shape
changes in terms of linear shift (Pucciarelli
et al., 1990): the neurofacial index measures
growth linearity between the neurocranium
and the face, while the pelviofemoral index
does so between the pelvis and the femur.
Food intake and water consumption were
estimated per animal/day. The monthly av-
erage values for maximum, medium, and
minimum temperature of the animal room
were also calculated. Humidity was assured
with a 1.0 ⫻ 0.5 ⫻ 0.5 m metallic reservoir
permanently filled with water. In this way
the environment was wetter when the tem-
perature increased and vice-versa. These
values, together with body weight, were em-
ployed as independent variables in the mul-
tiple regression analyses.
Differences in body weight at the begin-
ning of the experiment fluctuated between
425 g and 490 g in males, and 380 g and
455 g in females, i.e., by no more than 15%
and 20%, respectively. The frequency distri-
butions were tested by the one sample Kol-
mogorov-Smirnov (K-S) test. Results ranged
from DN ⫽ 0.085 in pelvic height of under-
nourished females to DN ⫽ 0.233 for neuro-
cranial index of control females. These re-
sults showed that the variables were
normally distributed (Table 1).
Correlation tests, and simple and multi-
ple regressions, were performed with the
Systat 7.0 statistical program. Curve fitting
procedures were carried out by the Table-
Curve 2D program (Jandel, 1994).
RESULTS
The monthly mean and standard devia-
tion values for body weight and femur
length in male and female control and mal-
nourished animals are shown in Tables 2
and 3, respectively.
Simple linear equation fitting
The constant values for adjusting each
component to the simple linear y ⫽ a ⫹ bx
equation are shown in Table 4. In four com-
parisons (neurofacial index in undernour-
ished males and pelviofemoral index in all
except control males), there were nonsignif-
icant Fm values. Consequently, the simple
regression model was invalidated in those
cases, and residual values were not regis-
tered. The determination coefficient (r2) ex-
plained more than 95% of the variation in
femur length for all the groups, and in the
pelvic index for control and undernourished
females (Fig. 1). The neurocranial and facial
indices in the four samples, the pelvic index
in males, the neurofacial index in control
males and control and undernourished fe-
 GROWTH OF SQUIRREL MONKEY SKELETAL COMPONENTS 61
1
TABLE 2. Descriptive statistics for body weight and femur length in male and female controls
Males Females
Femur length Femur length
Body weight (g) (mm) Body weight (g) (mm)
Age (months) X SD X SD X SD X SD
13 504.4 22.1 66.2 2.8 509.7 37.4 67.3 2.9
14 516.3 24.1 67.1 2.9 515.4 38.7 68.1 2.8
15 527.7 24.0 67.8 2.8 520.8 38.5 68.7 3.1
16 538.5 21.9 68.6 2.8 525.9 38.8 69.4 2.9
17 548.9 20.3 69.4 2.8 530.7 38.9 70.0 3.0
18 558.9 22.2 70.0 2.9 535.3 38.6 70.5 3.2
19 568.5 22.6 70.7 2.9 539.6 38.4 71.2 3.1
20 577.8 25.5 71.4 2.9 543.8 39.0 71.7 3.1
21 586.8 25.2 72.0 3.0 547.8 38.5 72.2 3.0
22 595.5 26.0 72.6 3.0 551.7 39.2 72.7 3.0
23 603.9 28.4 73.1 3.0 555.4 39.3 73.0 3.3
24 612.0 28.8 73.6 3.0 558.9 39.7 73.7 3.2
25 620.0 29.3 74.2 3.0 562.4 39.9 74.2 3.2
26 627.7 28.9 74.5 3.1 565.7 40.4 74.6 3.4
27 635.2 29.4 75.2 3.2 568.9 41.6 75.1 3.7
28 642.5 29.2 75.7 3.2 572.0 42.7 75.3 3.0
29 649.7 26.3 76.2 3.2 575.1 43.1 75.8 3.6
30 656.7 30.7 76.6 3.2 578.0 43.0 76.3 3.3
31 663.5 28.4 77.2 3.2 580.9 43.1 76.6 3.2
32 670.2 29.3 77.5 3.2 583.7 42.0 76.9 3.3
33 676.3 31.2 77.8 3.3 586.4 42.9 77.3 3.7
34 683.1 27.4 78.3 3.3 589.0 42.4 77.6 3.1
35 689.4 27.9 78.7 3.3 591.5 43.2 77.9 3.3
36 695.6 27.2 79.1 3.3 594.1 44.4 78.0 3.4
1
X, mean values; SD, standard deviations.

TABLE 3. Descriptive statistics for body weight and femur length in male and female undernourished animals1
Males Females
Femur length Femur length
Body weight (g) (mm) Body weight (g) (mm)
Age (months) X SD X SD X SD X SD
13 492.4 29.2 65.9 3.5 397.5 31.8 63.5 2.7
14 489.2 33.9 66.4 3.4 399.9 33.3 64.1 2.7
15 486.3 31.2 66.7 3.6 402.4 35.1 64.6 2.8
16 483.7 27.7 67.0 3.5 404.6 34.9 65.1 2.8
17 481.1 27.4 67.7 3.6 406.8 35.5 65.6 2.8
18 478.8 26.1 68.0 3.5 408.9 36.8 66.1 2.9
19 476.6 23.6 68.3 3.6 410.8 36.3 66.4 2.8
20 474.4 26.4 68.7 3.6 412.6 36.7 66.5 2.8
21 472.5 25.9 69.0 3.6 414.4 37.8 67.3 2.9
22 470.6 26.3 69.4 3.6 416.1 37.5 67.6 2.7
23 468.8 26.2 69.7 3.7 417.7 37.6 68.0 2.9
24 467.1 27.3 69.9 3.7 419.2 38.4 68.4 2.9
25 465.4 28.1 70.1 3.7 420.7 39.4 68.6 2.9
26 463.9 29.5 70.5 3.7 422.2 39.5 69.0 3.0
27 462.4 29.6 70.7 3.7 423.6 38.7 69.3 3.3
28 460.9 29.5 71.0 3.8 424.9 41.2 69.7 3.1
29 459.5 28.0 71.3 3.8 426.2 38.8 69.9 2.9
30 458.1 30.2 71.4 3.7 427.5 39.4 70.1 2.8
31 456.9 29.4 71.7 3.8 428.7 38.8 70.4 3.0
32 455.7 26.1 71.9 3.7 429.9 38.1 70.8 3.1
33 454.5 26.0 72.1 3.3 431.0 36.5 71.1 3.3
34 453.3 26.7 72.4 3.8 432.1 34.8 71.3 3.0
35 452.2 25.9 72.6 3.8 433.2 34.2 71.5 3.2
36 451.1 24.2 72.7 3.6 434.3 33.3 71.8 3.5
1
X, mean values; SD, standard deviations.
62 H.M. PUCCIARELLI ET AL.

TABLE 4. Bivariate analysis for femur length and indices1

Regression parameters ANOVA
Equation and group r r2 a ta b tb Fm RSS RMS
Equation: Y ⫽ a ⫹ bx
Control males
Femur length 0.995 99.0 64.4 169.2** 0.57 37.9** 1,435.9** 5.66 0.26
Neurocranial index 0.720 51.8 37.9 557.1** 0.06 22.1** 490.8** 0.18 0.01
Facial index 0.840 70.6 30.9 258.0** 0.09 19.3** 370.5** 0.56 0.03
Pelvic index 0.921 84.8 23.8 125.4** 0.14 18.7** 350.8** 1.41 0.06
Neurofacial index 0.878 77.1 81.7 285.9** 0.10 8.6** 74.2** 2.76 0.13
Pelviofemoral index 0.772 59.6 36.8 98.4** ⫺0.08 ⫺5.7** 59.9** 0.71 0.56
Control females
Femur length 0.996 99.2 65.9 205.6** 0.51 40.1** 1,609.6** 4.01 0.18
Neurocranial index 0.775 60.1 37.0 133.1** 0.07 5.9** 35.1** 3.02 0.40
Facial index 0.931 86.7 29.4 312.4** 0.11 28.7** 822.0** 0.93 0.04
Pelvic index 0.998 99.6 25.6 170.4** 0.19 31.9** 1,014.9** 0.88 0.04
Neurofacial index 0.680 46.2 80.0 123.0** 0.11 4.3** 18.6** 1.13 0.05
Pelviofemoral index ⫺0.245 6.0 39.0 121.9** ⫺0.02 ⫺1.2 1.5
Undernourished males
Femur length 0.977 95.5 65.0 140.7** 0.36 20.0** 397.9** 8.34 0.38
Neurocranial index 0.652 42.5 36.7 97.6** 0.10 6.8** 46.3** 5.52 0.25
Facial index 0.741 40.7 29.6 106.7** 0.09 8.7** 75.0** 3.01 0.14
Pelvic index 0.753 56.7 24.0 195.7** 0.06 12.3** 151.8** 0.59 0.03
Neurofacial index 0.341 11.6 80.7 144.7** 0.04 1.7 2.9
Pelviofemoral index ⫺0.351 12.3 35.0 59.9** ⫺0.04 ⫺1.7 0.1
Undernourished females
Femur length 0.981 96.2 62.8 149.0** 0.40 22.7** 516.4** 7.86 0.36
Neurocranial index 0.667 44.5 36.3 164.2** 0.09 10.8** 116.2** 1.90 0.09
Facial index 0.864 74.7 28.8 186.2** 0.11 17.4** 302.2** 0.93 0.04
Pelvic index 0.994 98.8 22.2 264.8** 0.17 50.9** 2,591.3** 0.27 0.01
Neurofacial index 0.570 32.5 79.9 168.2** 0.06 3.3** 10.6** 1.12 0.05
Pelviofemoral index 0.081 0.7 35.8 84.4** 0.02 0.8 0.7
1
r, correlation; r2, determination coefficient; a, intercept; b, slope; Fm, validity of the model; RSS, residual sum of squares; RSM,
residual mean of squares; **P ⱕ 0.01.

males, and the pelviofemoral index in con-
trol males, are all partially explained by the
simple regression equation. The unex-
plained fraction of the variation ranged
from 13% (facial index in control females) to
67% (neurofacial index in undernourished
females).
Tetra function equation type fitting
The variation fraction explained by the
curves ranged from 98.0% to 99.7%. The
unexplained variation was 1.3 % on aver-
age. The adjusted standard errors ranged
from 0.05 (neurocranial index in control
males) to 0.12 (pelvic index in control
males), and are low enough to reject any
significance of the residuals.

The components in which more than 5% of Multiple regression

the variation was not explained by simple
regression were fitted by one of the four
four-function equations with intercept of
the type y ⫽ a ⫹ bx ⫹ cf1(x) ⫹ df2(x) ⫹
ef3(x) (Table 5; Figs. 2, 3). The adjustment
was defined by the determination coefficient
(r2), and by both the variance analysis (Fm)
and the standard error (SEm) of the model.
The highly significant Fm values assessed
the validity of the regression model in all
comparisons: the smallest Fm was 169.1
(P ⬍ 0.01), for the pelvic index in under-
nourished males; and the greatest one was
1554.4 (P ⬍ 0.01), for the facial index in
undernourished females.
The multiple regression tests showed
which of the independent variables (factors)
acted on the patterns described by the four-
function equations (Tables 6, 7). The results
in Table 7 show the validity of the model
through the highly significant (P ⬍ 0.01) Fm
values. On average, the model explained
more than 99% of the variation, since the
determination coefficient range is 0.994
(neurocranial index) to 0.997 (pelvic index).
Six of the seven tested factors had (except
for age in neurocranial index) highly signif-
icant (P ⬍ 0.01) influence on old indices.
Water consumption was of lesser but signif-
 GROWTH OF SQUIRREL MONKEY SKELETAL COMPONENTS 63

Fig. 1. Example of simple linear growth in control females. The central straight line means that
growth explained more than 98% of the variation in femur length. The proximal lines are the confidence
intervals. The lateral ones limit the prediction intervals.

icant (P ⬍ 0.05) influence in all of the com-
parisons (Table 6).
DISCUSSION
There is consensus about the difficulty of
fitting linear equations to biological data
(Koops, 1986; Jolicoeur and Pirlot, 1988;
German et al., 1994). This is true not only
for simple regressions but also for more
complex linear relationships. The main
problem stems from the fact that growth is
neither a constant, nor an even or an infi-
nite process. It has a starting point (concep-
tion, birth), uneven velocity (growth spurts),
and asymptotic trends towards the end of
the growth period. Because of this complex-
ity, nonlinear equations are employed in the
study of long-lasting growth spans in mam-
mals with monosexual or bisexual spurts of
adolescence. Nonlinear exponential (Hiyaoka
et al., 1989; German et al., 1994); logistic
(Pearl, 1925; Bock and Thissen, 1976;
Preece and Baines, 1978; Lebeau et al.,
1986; Jolicoeur and Pirlot, 1988; Tanner,
1988; Hiyaoka et al., 1989); asymptotic
(Jolicoeur et al., 1988, 1992; Kanefuji and
Shohoji, 1990; Humphrey, 1998); and Low-
ess (Cleveland, 1979; Cleveland and Devlin,
1988; Efron and Tibshirani, 1991; Leigh,
1992, 1994, 1996) regression models, among
others, have been successfully employed for
studies in human and nonhuman primates.
An exception can be made in favor of the
linear models. When short periods of growth
are studied in genera such as Saimiri,
which does not display a plain growth spurt
in adolescence (Leigh, 1996), the linear
models are suitable and easier to interpret
than the nonlinear ones. Two main restric-
tions, however, have to be considered. First,
the linear equations define a line that ex-
tends infinitely in both directions. No mat-
64 H.M. PUCCIARELLI ET AL.

TABLE 5. Components of growth fitted by complex linear equations1

Group and ANOVA Regression parameters

equation (r2) SEm Fm a b c d e
x d e
Control males, equation: Y ⫽ a ⫹ bx ⫹ c ⫹ ⫹
lnx lnx x
Neurocranial index 99.0 0.05 468.8 14,640.9 173.1 ⫺1,049.4 ⫺44,287.8 74,533.6
Facial index 98.8 0.08 358.5 24,557.2 291.5 ⫺1,766.7 ⫺74,328.1 53,523.8
Pelvic index 98.9 0.12 396.2 23,350.7 271.8 ⫺1,653.9 ⫺71,011.9 119,732.5
Control females, equation: Y ⫽ a ⫹ bx ⫹ cx2 冑x ⫹ dx3 ⫹ ee⫺x
Neurocranial index 98.0 0.10 214.9 31.8 0.8 ⫺0.0 0.0 ⫺0.0
Facial index 98.3 0.11 275.5 26.4 0.5 ⫺0.0 0.0 ⫺0.0
d e
Undernourished males, equation: Y ⫽ a ⫹ bx ⫹ cx 冑x ⫹ ⫹
lnx x
Neurocranial index 99.3 0.08 715.6 6,523.7 ⫺57.4 4.3 ⫺23,103.4 39,872.4
Facial index 98.8 0.09 395.8 4,939.9 ⫺43.0 3.2 ⫺17,516.7 30,284.7
Pelvic index 98.2 0.08 169.1 ⫺1,486.5 14.1 ⫺1.1 5,352.5 ⫺9,213.1
x
Undernourished females, equation: Y ⫽ a ⫹ bx ⫹ cx 冑x ⫹ dx2 lnx ⫹ e
lnx
Neurocranial index 98.0 0.11 226.3 7,883.7 1,557.6 ⫺85.8 0.6 ⫺4,802.6
Facial index 99.7 0.05 1,554.4 3,162.3 619.1 ⫺33.8 0.2 ⫺1,913.8
1
The components of growth were fitted by the four four-function (b, c, d, e) standard linear equations with intercept (a), of the type
y ⫽ a ⫹ bx ⫹ cf 1( x) ⫹ df 2( x) ⫹ ef 3( x), with determination coefficient (r2), and ANOVA standard error (SEm), and significance
for the model (Fm).

ter how high or low a value of X is proposed,
the equation can predict a Y value. This
assumption is rarely reasonable in biologi-
cal data. Nevertheless, we can preserve the
model by employing the predictors of the
model only within the range of X values
defined by the experiment (Motulsky, 1995).
Second, the relationship between X and Y is
usually employed not to depict the best pos-
sible fit, but to know which proportion of the
variation can be explained by age as an in-
dependent variable. In these circumstances,
a simple regression equation has been suc-
cessfully employed in previous studies on
Saimiri (Hamano et al., 1990; Dressino,
1991; Dressino and Pucciarelli, 1997, 1999).
Neural structures such as the brain and
the eyes show fast early growth, with the
structures approaching adult size during
childhood. The body organs, however, follow
general somatic trends and reach adult size
after puberty (Humphrey, 1998). These pat-
terns are observed in the results obtained in
the present study. The growth of Saimiri
skeletal functional components was de-
scribed by three different patterns. 1) The
simple linear one comprised components
whose variability was entirely explained
(r2 ⱖ 95%) by the Y ⫽ a ⫹ bx equation.
These components were femur length in
control and undernourished males and fe-
males, with the highest regression slopes
(bx ⫽ 0.46), and the pelvic index in control
and undernourished females, with medium
slope values (bx ⫽ 0.18). 2) The complex
linear pattern involved components with an
average of 40.8%of the variation unex-
plained by the simple regression, with the
smallest regression slopes (bx ⫽ 0.09). The
highest percentages of explanation (r2 ⱖ
95%) were obtained by four four-function
standard linear equations of the type: y ⫽
a ⫹ bx ⫹ cf1(x) ⫹ df2(x) ⫹ ef3(x). Each
equation described the growth of the compo-
nents from one specific group. Conse-
quently, the components are genetically
(sex) and environmentally (nutrition) influ-
enced (Table 5; Figs. 2, 3). 3) The noncorre-
lated with age pattern was reserved for mor-
phometric indices that test the linearity of
growth between the components. Hence,
these indices were not included in the fitting
of complex linear equations. Their nonsig-
nificant simple regression models stated,
e.g., that a linear relationship of growth ex-
ists between the pelvis and the femur. On
the other hand, linear growth between the
neurocranium and the face was absent,
since significant regression models were
found in most of the cases.
In this study, the null hypothesis pro-
posed that all major skeletal components of
 GROWTH OF SQUIRREL MONKEY SKELETAL COMPONENTS 65

Fig. 2. Example of complex linear growth in control males. The central curved line means that growth
explained about 97% of the variation in neurocranial components. The proximal lines are the confidence
intervals. The lateral ones limit the prediction intervals.

the platyrrhine body grow linearly, regard-
less of different demands for different func-
tions. Accepting the null hypothesis implies
that linear growth in the skeletal frame of
Saimiri would be expected. The results,
however, allowed us to reject the hypothe-
sis. The skeleton did not grow evenly but
according to functional demands imposed by
related soft tissues and body cavities. The
simple linear pattern seen in the femur of
both sexes may be linked to the steady
growth in height of the young animals. The
same may occur in the female pelvic index,
maintaining the normal bony conditions for
parturition, in both the control and stressed
environments.
Because complex linear equations were
necessary for explaining skeletal growth, a
nongenetic mechanism influences growth in
the Saimiri genus. This implies that factors
independent of age were acting. Age incre-
ments explained only part of the variation
in the complex linearly patterned compo-
nents. The remainder of the variation was
due to the sum of other independent vari-
ables. Because the sinuous trajectory found
in the complex linear components is not an
artifact (Jandel, 1994), eco-geographical fac-
tors may explain this pattern. For example,
several observations have been made about
the intraspecific differences in size due to
the latitude, habitat, and rainfall affecting
Macaca (Albrecht, 1978, 1980; Hamada et
al., 1986; Albrecht and Miller, 1993; Fooden
and Albrecht, 1993; Turner et al., 1997) and
Callithrix (Albrecht, 1982) genera. This sug-
gests that eco-geographic variation in pri-
mates may be multifactorial, i.e., with differ-
ent factors influencing different situations.
The strong oscillation in environmental tem-
perature, food intake, and body weight seen in
our experiment on squirrel monkeys corre-
66 H.M. PUCCIARELLI ET AL.

Fig. 3. Example of complex linear growth in undernourished females. The central curve line means
that growth explained more than 99% of the variation in facial components. The proximal lines are the
confidence intervals. The lateral ones limit the prediction intervals.

TABLE 6. Multiple regression tests for total sample

Body Food Water Environmental
Index Age Sex weight intake intake temperature
Neurocranial 1.0 7.3** 21.9** 13.3** 3.9** 2.4*
Facial 5.4** 11.2** 14.9** 3.5** 4.1** 2.3*
Pelvic 6.5** 3.6** 21.3** 2.2** 2.9** 2.1*
* P ⬍ 0.05.
** P ⬍ 0.01.

sponds to that of the tropical forest in which TABLE 7. Adjusted ANOVA for multiple
regression model1
significant seasonal variation occurs. The
cool-rainy season (winter) lasts from Decem- Index MS SE F Adj.r2 D-W
ber to April, and the warm-dry one (summer) Neurocranial 31,725.6 6.4 4,926.0* 99.4 6.441
from May to November (Murrieta et al., Facial 43,601.5 5.3 8,279.3* 99.6 2.295
Pelvic 22,007.6 2.2 9,951.4* 99.7 0.513
1989). Alternate conditions make food produc-
1
tion and food reserves cyclic (Rosenblum and MS, mean square values; SE, standard error of the mean
squares; F, F significance of indices; Adj.r2, adjusted determina-
Coe, 1985). The dry season, with high temper- tion coefficients expressed as percent; D-W, Durbin-Watson test.
* P ⬍ 0.01.
atures, low relative humidity, and food scar-
city, might decrease growth rates, which are
responsible for the lowest slopes of the four- availability of food, might increase growth
function curves. The rainy season, with mod- rates, which are responsible for the highest
erate temperatures and greater quality and slopes of the complex linear equation curves.
 GROWTH OF SQUIRREL MONKEY SKELETAL COMPONENTS
In fact, the simple linear growth components
also suggest an undulating trend, although
masked by the high growth rate of the com-
ponents involved (see Fig. 1).
CONCLUSIONS
The null hypothesis tested in the present
experiment was rejected in regard to the
following considerations.
1. The skeletal components of the squirrel
monkey behaved according to two de-
fined patterns of growth. The femur in all
of the groups, and the pelvis of the fe-
males, grew straight and fast. The face
and the neurocranium in all of the
groups and the pelvis of the males grew
slowly and in an undulating fashion.
These growth modalities were imposed
by several different functional demands.
The neurocranium and the face grew
mostly during lactation. In the present
experiment, only the final growth stages
of these two components were detected,
each with a feeble increment, and having
a nonlinear relationship between them.
The femur went on growing actively, fol-
lowing the increment in stature. Sexual
dimorphism was evident in the growth
pattern of the pelvis. The linear growth
showed by the pelviofemoral index is in-
terpreted as a greater pelvic growth rate
in females than in males, presumably to
ready the female organism for reproduc-
tive activity.
2. Undernutrition affected growth in height
in both sexes and pelvic growth only in
males. The pelvis in females and the neu-
rocranium and the face in both sexes
were not affected. This fact reinforced
the idea of functional demands acting on
growth. The skull components were pro-
tected from undernutrition due to their
early growth. The “better pelvic growth
canalization of the females” may be
closely related to reproduction.
3. The undulating growth trend observed in
the complex linear growing components
might be related to the feeding behavior
of the primates of the tropical forest. The
rising slopes of the four-function curves
may be evoked in the rainy season, when
food quality and quantity are better than
in the dry one. The downhill slopes may
67
be evoked during the dry season, when
food quality and quantity generally turn
poorer than in the rainy season.
ACKNOWLEDGMENTS
The authors are grateful to Med. Vet.
Daniel O. Arias from Servicio de Cardiologı́a
(FCV, UNLP) for his useful help in the
health care of the experimental animals;
and to Miss. Damiana C. Pucciarelli for her
highly valuable assistance in the transla-
tion of the present manuscript.
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